Journal of the American Control Association, l5(2):ll7-127, 1999 Copyright O 1999 by the American Association, Inc.

A HISTORICAL REVIEW OF THE F-l STRAIN OF FREEBORNI AS A HOST AND VECTOR FOR STUDIES OF

WILLIAM E. COLLINS AND GEOFFR-EY M. JEFFERY

Divisktn of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Service, U.S. Department of Health and Humnn Services, Atlanta, GA 30341

ABSTRACT. A reveiw was made of the use of a specific strain of from California (F-1) that has been used extensively in experimental investigations ofmalaria for more than 50 years. The F-l strain of An. freeborni has been shown to be a suitable experimental host and vector for different species of that cause malaria in humans and nonhuman primates for biologic, immunologic, and chemotherapeutic studies. Eleven species of Plasmodium ftlly completed sporogonic development; development of sporozoites within mature oocysts occurred in an additional 7 species. Transmission through An. .freeborni from human to human, monkey to human, or monkey to monkey has been demonstrated for 9 species of Plasmodium.

KEY WORDS Anopheles freeborni, Plasmodium, malaria, mosquitoes

INTRODUCTION Plasmodium. A review of the use of this mos- quito for studies with human and nonhuman pri- Over the last half century, several species of mate malaria parasites indicates that this is a re- anopheline mosquitoes have served as laboratory markably usefi.rl vector for biologic, immunologic, hosts for experimental studies on malaria. Among and chemotherapeutic studies. these are Anopheles quadrimaculatus Say, An. atroparvus Thiel, An stephensi Liston, An. albi- manus Wiedemann, and An. freeborni Aitken. HUMAN MALARIA PARASITES Here we summarize some of the studies that have established An. freeborni as one of the most use- The earliest studies with the F-l strain in- ful and suitable hosts for a variety of investiga- volved the feeding of colony-reared mosquitoes tions of malaria. on -infected soldiers returning The F-l strain of An. (An.) freeborni Aiken from the South Pacific and the Mediterranean was established from eggs laid by wild-caught fe- during World War II. Young et al. (1945) reported males collected near Marysville, CA, on March that 1,358 of 2,581 mosquitoes that fed on these 3, 1943. The colony was supplemented by an ad- patients became infected; several infections with ditional 800 wild-caught females on March 15 P. vivax originating from the Pacific were exper- and 25O to 400 females collected from the same imentally transmitted by An. freeborni. Moore et location on April 30, 1943. On August 21, 1944, al. (1945) reported on the feeding of 64 lots of eggs were shipped from the U.S. Public Health An. freeborni on relapsing P. vivax infections in Service laboratory at Letterman General Hospi- soldiers. Mosquitoes became infected and 8 in- tal, San Francisco, CA, to the U.S. Public Health fections were transmitted to other patients by this Service laboratory in Columbia, SC. This was vector. Oocyst counts as high as 8OOper gut were "Imported part of the wartime Malaria Studies" found, although the usual oocyst counts ranged effort to determine the potential of native anoph- from 1 to 24. Hardman (L947) summarized the elines to transmit malaria parasites from infected procedures being used at that time for the labo- returning servicemen. Since its establishment, ratory rearing of these mosquitoes. These early this strain of An. freeborni l;.as been maintained studies indicated that An. freeborni had high po- continuously in various laboratories where it has tential for more extensive investigations. Of early served as the standard host and vector for com- interest was the relative efficiency of different parative studies with many species of Plasmodi- laboratory-reared anopheline vectors in transmit- um causing human and nonhuman malaria. ting different species and strains of human ma- A suitable experimental host and vector should laria parasites. Using simultaneous feedings, be able to be reared in relatively large numbers Young and Burgess (1948) reported on the com- using standard insectary techniques, should read- parative susceptibility of An. quadrimaculatus ily feed on or human hosts, should sup- from the southeastern United States and An. free- port sporogonic development to the production of borni from California to foreign vivax malaria; infectious sporozoites, and should be capable of their studies indicated that the latter was more transmitting the infection by feeding on a suscep- susceptible (more oocysts per gut and higher per- tible host. Preferably, a laboratory vector will be centage of infection). Young et al. (1948) report- susceptible to infection with and be capable of ed the infection of An. freeborni witln P. vivax transmitting a number of different species of from different geographic origins, including the Il]]]

u8 JounNnLon rne AvnnrcaN Mosqurro CoNrnol AssocrATroN Vor-. 15, No. 2

Table 1. Studies on the infection and transmission of Plasmodium vivax, P. falciparum, p. malariae, and.p. ovale by Anophe les freeborni. Species of Plasmodium Strains (geographic origin) Primate hosts References P. vivax South Pacific and Meditera- Humans, night monkeys, Moore et al. 1945; Young nean, Sal I and Sal II (El squirrel monkeys, chim- et al. 1945, 1948; Young Salvador), Chesson (New panzees and Burgess 1948; Bur- Guinea), West Pakistan gess and Young 195O; (Pakistan), ONG and Collins and Roberts NAM (Indonesia), St, 1991: Collins et al. Elizabeth (U.S.A.), NICA 1969c, 1972b, 1973c, (Nicaragua), Panama 1973d, 1974c, 1976a, (Panama), Vietnam I-IV 1976b, 1977a, 1979a, (Vietnam), Vietnam Palo 1979d, 1980a, 1980b. Alto (Vietnam), Brazll U 1980c. 1983a. 1985b. CDC (Brazil), Mauritania 1985c, 1985e,1986a, VCDC (Mauritania), New 1986c, 1987b, 1987d, Guinea (New Guinea), 1988, 1992b, 1994a, North Korean (Korea), 1998a, 1998b; Coatney et India VII (India), and al. 1971t Singal et al. others 1977; Warren and Collins 1981; Krotoski et al. 1982; Campbell et al. 1983: Wirtz et al. 1985: Hollingdale et al. 1985, 1986; Millet et al. 1989; Porter and Collins 1990; Barr et al. l99l; Chareno- vit et al l99l; Sullivanet al. 1996; Nayar et al. 1997 P. falciparum Mclendon (U.S.A.), Pana- Humans, night monkeys, Beier et al. 19921,Burgess ma II (Panama), Santa squirrel monkeys, chim- and Young 1946; Burkot Lucia (El Salvador), Ma- panzees et al. 1984; Campbell et layan IV (Malaysia), al. 1980a, 1980b, 1982, Cambodian I (Cambodia). 1986; Chege et al. 1996; West Africa I (Nigeria), Collins et al.1963, NF-54 and 3D7 (Nether- 1964a, 1968b, 1972, lands). and Indochina I 1973e, 1973f, 19'77a, (Thailand-Cambodia), 1977b, 1978, r979a, Burma Thau. (Burma), 1979c, 1979d, 1981a, Montagnard (Vietnam), 1982a,1982b, 1983b, Colombia (Colombia), 1986d, 1991, 1996a, Thailand (Thailand), El 1996b. 1997b: Contacos Limon (Panama), and and Collins 1968; Sode- others man et al. 1969; Coatney et al. 1971; Chin and Collins 1980; Collins and Contacos 1980; Ponnudu- rai et al. 1982; Mazier et al. 1984; Techlehaimanot et al. 1987; Graves et al. 1988: Renia et al. 1988: Do Rosario et al. 1989: Millet et al. 1991a; Sha- habuddin et al. 1993; Vaughn et al. 1994a, 1994b; Noden et aI. 1995; Vaidya et al. 1995; Gozar et al. 1998

Solomon Islands, New Guinea, New Britain, the susceptible than was An. quadrimaculatus. This Mediterranean, Burma, and the Carribean. Bur- strain, of probable U.S. origin, was frequently gess and Young (1950) reported on a comparative used for the induction of malariotherapy of pa- study on the susceptibility of An. quadrimacula- tients with neurosyphilis, a standard treatment at tus and An. freeborni to the St. Elizabeth strain that time. With the cessation of the use of malaria of P. vivax. Here again, An. freeborni was more for the treatment of neurosyphilis, studies on JUNE1999 HISToRICAL REvIEw oF ANoPHELES FREEBORNI ll9

Table 1. Continued.

Species of Plasmodium Strains (geographicorigin) Primate hosts References P. malariae USPHS (U.S.A.), Philip- Humans, night monkeys, Young and Burgess 1961; pines, Nigeria, Uganda, squirrel monkeys, chim- Collins and Contacos China I/CDC Danzees 1969: Contacos and Col- lins 1969; Coatney et al. 1971; Collins et al. 1973a, 1975a, 1984a, 1989a, r989b, l99Od, 1994b. 1997a:.Millet et al. 1988a: Nagasawa et al. 1988 P. ovale Donaldson (South Pacific), Humans, chimpanzees Chin et al- 1966: Collins et West Africa, Nigerian a1. I969c. 1987c: Coat- ney et al. l97l; Mazier et al. 1987; Nagasawa et al. 1987; Millet et al. 1994; Morris et al. 1996

transmission to humans ceased. With the subse- experimental studies with P. ovale and An. free- quent establishment of P. vivax in New World borni have also been conducted in chimpanzees. monkeys, a large number of different isolates and Different strains of this parasite readily infect An. strains of P. vivax were now available for studv freeborni, and exoerythrocytic (liver stages) of it An. freebornl (Table 1). the parasite have been demonstrated in squirrel Burgess and Young (1946) were the lst to re- monkeys (Saimiri spp.). However, no erythrocyt- port the experimental transmission by An. free- ic-stage infections have been established in New borni of (Mclendon World monkeys. strain) to 2 patients; prepatent periods were 15 The ready infectivity of many different strains and 29 days. Anopheles freeborni then became of human malaria parasites from diverse geo- one of the standard hosts and vectors for trans- graphic areas to An. freeborni suggested that this mission studies with this parasite. Jeffery et al. mosquito could serve as a universal host for a (1963) reported on studies with a multidrug-re- variety of chemotherapeutic and immunologic sistant strain of P. falciparum from Thailand in studies. In fact, this has become the case in sev- which 6 patients were infected via the bites of eral laboratories in the United States. An. freeborni. In a comparative susceptibility study based on oocyst densities, Collins et al. NONHUMAN PRIMATE (L964a) demonstrated that, with a strain of P. MALARIA fal- PARASITES ciparum from Panama, An. freeborni was more heavily infected than was An. quadrimaculatus or Monkeys have long been used a models for even a coindigenous strain of An. albimanus. chemotherapeutic and immunologic studies with However, the adaptation of various strains of P. malaria parasites, and both Old World and New falciparum to New World monkeys opened up a World monkeys have been infected with various new field of study where An. freeborni was ex- species of Plasmodium. For almost 40 years, we posed to isolates and strains of the parasite from have usedAn. freeborni as a laboratory vector for distant geographic areas (Table 1). a variety of studies on malaria in nonhuman pri- was first shown to be mates (Table 2). It early became apparent that, transmissible by An- freeborni by Young and although in most instances An. freeborni was Burgess (1947). Little further success in the highly susceptible to the development of the oo- transmission of this parasite was obtained until cyst stage, some species of Plasmodium failed to Contacos and Collins (1969) reported the trans- develop to the point of sporozoites being present mission of P. malariae from an infected night in the salivary glands. With all but a few species, monkey (Aotus sp.) to humans. Although subse- oocyst densities in An. freeborni were high; oo- quent studies indicated monkeys and chimpan- cyst counts could be used as an indicator of ga- zees would support the development of p. ma- metocyte infectivity. However, transmission via lariae gametocytes infective to An. freeborni, sporozoites could only be obtained if oocysts transmission via sporozoites to other monkeys containing mature sporozoites were crushed and and chimpanzees was not successful. then injected into the primate. Plasmodium cy- Chin et al. (1966) reported the transmission of nomolgi, P. gonderi, P. simium, P. fragite, and a West African strain of from P. brasilianum, parasites of monkeys, developed human to human using An. freeborni. Successful fully, including the presence of sporozoites in the 120 JounNnl on tHe AlvrnnrclNMosqurro Corqrnol AssocterroN Vor-. 15, No. 2

Table 2. Studies on the infection and transmission of nonhuman primate-infecting species of Plasmodium by Anopheles freeborni. Species of Plasmodium Strains (geographic origin) Primate hosts References P. brasilianum S (Colombia), AT (Pana- Night monkeys, squirrel Collins et al. 1969b, ma) Peruvian I-III monkeys, spider mon- 1985d, 1990b, 1993; So- keys, humans deman et al. 1969; Coat- ney et al. l97l P. coatneyi Hackeri (Malaysia) Macaques Held and Contacos 1967; Coatney et al. l97l;' Coffins et al.1992a P. crynomolgi B, Berok, M, Gombak Macaques, night monkeys, Coatney et al. 1971; Col- (Malaysia), ceylonensis squirrel monkeys lins et al. 1972c, l9'15b, (Sri Lanka), RO (As- 1985a, 1998; Krotoski et sam-Burma), Celebes al. 1973: Omar and Col- (Philippines), Cambodi- lins 1973; Omar et al. an 1973, 1974:' Atkinson et al. 1989; Millet et al. 1989,1990 P. fieldi Hackeri, N-3, ABI, Malay- Macaques Coatney et al. 1971; Col- sian lins et al. 1984b,1992a P. fragile Sri Lanka, Nilgiri (India) Macaques, Night monkeys, Collins et al. 1967, 1974b, squirrel monkeys 1975c, l990a, 1992a; Coatney et al. 19'71 P. gonderi Mandrill (West Africa) Macaques Collins et al. 1964b, 1992a; Coatney et aI. 1971; Collins and Con- tacos 1980 P. hylobati WAK (Indonesia) Gibbons Coatney et al. l97l; Col- lins et al. 1972d P. inui Taiwanland2(Taiwan), Macaques, night monkeys, Collins et al. 1968a, N-34, Perlis, Perak, I-eaf squirrel monkeys 198lb; Held et al. 1968; Monkey I and II, ku- Coatney et al. l97l:' cosphyrus, Mulligan, Nguyen-Dinh et al. and others (Malaysia), 1980; Collins and War- OS (India) ren 1998 P. jefferyi Malaysian Gibbons Collins and Orihel 1969; Coatney et al. 1971; Ro- denberg 1985; Millet et al.1988b P. knowlesi H, Malaysian, Hackeri Macaques, humans, night Coatney et al. 19'71 (Malaysia) monkeys, squirrel mon- keys P, reichenowi Chimpanzee (West Africa) Chimpanzees Coatney et al. 1971; Col- lins et al. 1986b P. schwetzi Chimpanzee (West Africa) Chimpanzees, humans Collins et al. 1969c; Con- tacos et al. 1970; Coat- ney et al. t97l P. simiovale Sri Lanka Macaques Coatney et al. l97l; Col- lins et al. 1972a,1992a; Collins and Contacos 1979 P. simium Howler (Brazil) Night monkeys, squirrel Collins et al.1969a, monkeys 1973b, 1974a, 1979b, 1987a; Coatney et al. 197 |

salivary glands of An. freeborni. Plasmodium transmission could be obtained only through the schwetzi and P. reichenowi, parasites of chim- injection of mechanically harvested sporozoites. panzees and gorillas, and P. hylobati, a parasite Those parasites requiring mechanical harvesting of gibbons, also developed to maturity in this included , P. simiovale, P. vector. coatneyi, P. fieldi, and P. inui. Some parasites failed to develop beyond the Anopheles freeborni has been shown to support presence of mature sporozoites in oocysts and the complete sporogonic development of many Juxe 1999 HISToRICAL Rgvrsw oF ANoPHELES FREEBoRNI

sPoRozotTEs SPOROZOIIESIN SALIVARYGLANDS tN oocYsTs

70 '15 11 ?? 12 11 12 13 12 14 17 17 12r 12' 14' 14' 13* 161 16r a 260 o E eQso cr40 -UJ lil =30 o20 z uJ .^

0 cynomolgi gondei lalcipmm simium reichenowimaliliae knowl$i simiovale ietleN inui schweai viw Wobati Nah brcilimm coatneyi tieldi lngile SPECIESOF PIASMODIUM Qaoevs!roorvs ffirzorvsffir+onvs Fig. l. Mean oocyst diameter at 8, 10, 12, and 14 days and days when sporozoites are present in salivary glands or mature oocysts inAnophelesfreeborni mosqtoitoes infected with 18 species of Plasmodium when incubated at 25 + 1"C.

different species of Plasmodium, but fails to do j"ff"ryi, P. fieldi, P. simiovale, and P. coatneyi; so for other parasites (Fig. 1). This mosquito the quartan parasite P. inui; and the quotidian readily supports full development, to the pres- parasite P. knowlesi. In these latter species, in- ence of sporozoites in the salivary glands, of P. fective sporozoites are present in mature oocysts, vivax and P. ovale and the related nonhunman but are rarely found in the salivary glands. Infec- tertian parasites P. cynomolgi, P. gonderi, P. tivity of these sporozoites has been demonstrated schwetfi, and P. simium; P. falciparum and the by the injection of susceptible hosts with sporo- related parasite P. reichenowi; P. malariae and zoites mechanically released from mature oo- the related quartan parasite P. brasilianum: and cysts. In our studies with monkeys (Table 3), the tertian parasite P. hylobati. Anopheles free- transmission via bite or the injection of sporo- borni supports to a lesser extent the sporogonic zoites dissected from An. freeborni has been development of the tertian parasites P. fragile, P. demonstrated with 9 species of Plasmodium. Be-

Table 3. Transmission of 9 species of Plasmodium from monkey to monkey by Anopheles freeborni mosquitoes.

Transmissions Prepatentperiod(days) Species of Plasmodium Donor Recipient Bite Injectionr Range Median P. brasilianum Saimiri Saimiri 90t8-42 34.O Ateles Ateles 30t8-43 36.0 P. coatneyi Macaca mulatta M. mulatta 0614-15 15.0 P. cynomolgi M. mulatta M. mulatta 32 8-36 I1.0 a1 8-24 9.0 Aotus Aotus 30l5-19 18.0 P. falciparum Aotus Aotus 44 10-69 23.O 8 t6-69 22.O P. fieldi M. mulatta M. mulatta 03l8-30 18.0 P. gonderi M. mulatta M. mulatta 100 t2-17 13.0 P. inui M. mulatta M. mulatta o2t2-15 13.5 P. knowlesi M. mulntta M. mulatta 035-6 6.0 P. vivax Aotus Aotus 37 14-55 2t.o a 1417 20.s Aotus Saimiri l0 39 39.0 Samiri Saimiri 0l 28 28.0 'Intravenous or intrahepatic injection of sporozoites dissected from omysts or infected salivry glands. 122 JounNll oF THE AMERlc,rN Mosquno CoNrnol AssocrATloN Vol. 15,No.2 cause of the invariable success in all species test- of cultured Plasmodium falciparum. Trans. R. Soc. ed, there is no reason to believe that sporozoites Trop. Med. Hy g. 74:668-669. from salivary glands or mature oocysts of the Campbell, C. C., W. E. Collins, J. M. Roberts and A. other species of human and nonhuman primate Armstead. 1986. Adaptation of the Indochina VCDC stratn of Plasmodium to the squirrel monkey malaria parasites produced in An. could falciparum freeborni (Saimiri sciureus). Am. J. Trop. Med. Hyg. 35:472-475. not also be infective to susceptible primate hosts. Campbell, C. C., H. C. Spencer, W. Chin and W. E. Cot- Ano p he I es fre eb o rni, after long-term establish- lins. 1980b. Adaption of cultured Plasmodiumfalcipa- ment in the laboratory, has been shown to be rum to the intact squirrel monkey (Saimiri sciureus). highly susceptible to many species of Plasmodi- Trans. R. Soc. Trop. Med. Hyg. 74:548-549. um from widely separated geographic areas. In Campbell, C. C., W. Chin, W. E. Collins, S. M. Teitsch addition, the susceptibility to many different and D. M. Moss. 1979. Chloroquine-resistant Plasmo- strains of the parasites from widely separated dium falciparum from East Africa. Lancet 1:1151- geographic areas allows us to use this mosquito 1t54. Campbell, C. C., W. E. Collins, W. Chin, J. M. Roberts as a standard for all studies with human malaria and J. R. Broderson. 1983. Studies on the Sal I strain parasites and most of the nonhuman-infecting of Plasmodium vivrtx in the squirrel monkey (Saimiri species. sciureus). J. Parasitol. 69:598-601. Many questions remain concerning the rela- Campbell, C. C., W. E. Collins, P Nguyen-Dinh, A. Bar- tionship between this mosquito host and the dif- ber and J. R. Broderson. 1982. Plasmodiumfalciparum ferent species of human and nonhuman primate gametocytes from in vitro culture develop to sporozo- malaria parasites. The reasons why one species ites which are infectious to primates. Science 217: of Plasmodiun develops completely, whereas an- 1048-1050. Y., other does not, deserves investigation. Why are Charoenvit, W. E. Collins, T, R. Jones, P. Millet, L. Yuan, G. H. Campbell, R. L. Beaudoin, J. R. Broderson oocyst densities higher in An. than rn freeborni and S. L. Hoffman. 1991. Inability of other mosquitoes when simultaneously fed on to induce antibodies to a protective epitope within its certain strains of Plasmodium? Why is the re- sequence. Science 251:668-67 l. verse true with other species and strains of par- Chege, G. M., C. B. Pumpuni and J. C. Beier. 1996. Pro- asites when different species of anophelines si- teolytic enzyme activity and Plasmodium falciparum multaneously feed on the same animal? The sporogonic development in three species of Anopheles extensive data available from studies on the F-l mosquitoes. J. Parasitol. 82: I 1-16- Chin, W. and W. E. Collins. 1980. 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